Skip to main content
SpringerLink
Log in

The reproductive ecology of the invasive ascidian, Styela clava, in Auckland Harbour, New Zealand

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The ascidian Styela clava, native to the north-west Pacific, is an invasive species affecting New Zealand’s marine ecosystems, biodiversity and aquaculture operations. To provide detailed information on the reproductive biology of S. clava in New Zealand for post-border biosecurity management, long-term seasonal patterns of gametogenesis were determined from May 2006 to May 2008 in Auckland’s Waitemata Harbour (36°49′20″S, 174°45′85″E). Of particular interest was whether the critical 15°C threshold spawning temperature for reproduction observed in the Northern Hemisphere applied here to the first Southern Hemisphere study. S. clava gametogenesis followed a regular seasonal cycle with ripe gametes appearing as early as September and persisting to June; this time frame corresponds to the period when sea surface temperatures in the region first reach 15°C and with spawning occurring mainly during late summer to early autumn. From photoperiod manipulation, it was determined that spawning occurred at approximately 18:20. The extended reproductive period and a short generation time in the Waitemata Harbour provides a lengthy opportunity for S. clava to spread. Findings are discussed in relation to S. clava’s post-border management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbott DP, Johnson JV (1972) The ascidians Styela barnharti, S. plicata, S. clava, and S. montereyensis in Californian waters. Bull South Calif Acad Sci 71:95–105

    Google Scholar 

  • Agius BP (2007) Spatial and temporal effects of pre-seeding plates with invasive ascidians: growth, recruitment and community composition. J Exp Mar Biol Ecol 342:30–39

    Article  Google Scholar 

  • Atkins J (2009) Leigh marine laboratory’s long term monitoring programme. Leigh Marine Laboratory, University of Auckland

  • Bax N, Carlton JT, Mathews-Amos A, Haedrich RL, Howarth FG, Purcell JE, Rieser A, Gray A (2001) The control of biological invasions in the World’s Oceans. Conserv Biol 15:1234–1246

    Article  Google Scholar 

  • Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323

    Article  Google Scholar 

  • Blum JC, Chang AL, Liljesthröm M, Schenk ME, Steinberg MK, Ruiz GM (2007) The non-native solitary ascidian Ciona intestinalis (L.) depresses species richness. J Exp Mar Biol Ecol 342:5–14

    Article  Google Scholar 

  • Bourque D, Davidson J, MacNair NG, Arsenault G, LeBlanc AR, Landry T, Miron G (2007) Reproduction and early life history of an invasive ascidian Styela clava Herdman in Prince Edward Island, Canada. J Exp Mar Biol Ecol 342:78–84

    Article  Google Scholar 

  • Bullard SG, Lambert G, Carman MR, Byrnes J, Whitlatch RB, Ruiz G, Miller RJ, Harris HL, Valentine PS, Collie JS, Pederson J, McNaught DC, Cohen AN, Asch RG, Dijkstra J, Heinonen K (2007) The colonial ascidian Didemnum sp. A: current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. J Exp Mar Biol Ecol 342:99–108

    Article  Google Scholar 

  • Carlisle DB (1945) Styela mammiculata N.SO. A new species of ascidian from the Plymouth Area. J Mar Biol Ass UK 33:329–334

    Article  Google Scholar 

  • Carlton JT (1985) Transoceanic and inter-oceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol 23:313–371

    Google Scholar 

  • Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–273

    Article  Google Scholar 

  • Carlton JT, Geller J (1993) Ecological roulette: the global transport of non-indigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a midintertidal rocky shore. Mar Ecol Prog Ser 268:119–130

    Article  Google Scholar 

  • Chang FH, Zeldis J, Gall M, Hall J (2003) Seasonal and spatial variation of phytoplankton assemblages, biomass and cell size from spring to summer across the north-eastern New Zealand continental shelf. J Plankton Res 25:737–758

    Article  CAS  Google Scholar 

  • Clarke CL, Therriault TW (2007) Biological synopsis of the invasive tunicate Styela clava (Herdman 1881). Can Manus Report Fish Aquatic Sci 2807:vi + 23

  • Clavero M, García-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110

    Article  Google Scholar 

  • Coutts ADM, Forrest BM (2005) Evaluation of eradication tools for the clubbed tunicate Styela clava, Cawthron Report vol. 1110. Cawthron Institute, Nelson

  • Coutts A, Moore K, Hewitt C (2003) Ships’ sea chests: an overlooked transfer mechanisms for non-indigenous marine species? Mar Pollut Bull 46:1504–1515

    Article  Google Scholar 

  • Davidson J, Arsenault G, MacNair N, Landry T, Bourque D (2005) Reproduction, epidemiology and control of the clubbed tunicate, Styela clava. In: Prince Edward Island waters. Aquaculture and Fisheries Research Initiative Report Number 043AR15

  • Davis MH (1997) Physical factors influencing larval behaviour in three species of solitary ascidian. PhD Thesis, Department of Biology, Open University, Milton Keynes

  • Davis MH, Davis ME (2005) Styela clava (Tunicata: Ascidiacea) a new addition to the fauna of the Portuguese coast. J Mar Biol Assoc UK 85:403–404

    Google Scholar 

  • Davis MH, Davis ME (2006) Steyla clava (Tunicata: Ascidiacea) a new addition to the fauna of New Zealand. Porcup Mar Nat Hist Soc Newslett 20:23–28

    Google Scholar 

  • Davis MH, Davis ME (2007) The distribution of Styela clava (Tunicata, Ascidiacea) in European waters. J Exp Mar Biol Ecol 342:182–184

    Article  Google Scholar 

  • Davis MH, Davis ME (2010) The impact of the ascidian Styela clava Herdman on shellfish farming in the Bassin de Thau, France. J Appl Ichthyol 26:12–18

    Article  Google Scholar 

  • Denny CM (2008) Development of a method to reduce the spread of the ascidian Didemnum vexillum with aquaculture transfers. ICES J Mar Sci 65:805–810

    Article  Google Scholar 

  • Ehrlich PR (1989) Attributes of invaders and the invading processes: vertebrates. In: Drake JA, Mooney HA, DiCastri HA, Groves HA, Kruger FJ (eds) Biological invasion: a global perspective. Wiley, New York, p 525

    Google Scholar 

  • Elton CS (1933) Alien invaders: an animal census in Britain. The economics of wild life. London Times, May 6, 1933

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London

    Google Scholar 

  • Giese AC (1958) Comparative physiology: annual reproductive cycles of marine invertebrates. Annu Rev Physiol 21:547–576

    Google Scholar 

  • Giese AC, Kanatani H (1987) Maturation and spawning. In: AC Giese, JS Pearse, Pearse VB (eds) Reproduction of marine invertebrates, vol IX. Blackwell, Palo Alto, pp 251–329

  • Goddard CK, Hoggett AK (1982) Gut contents of the ascidian Pyura praeputialis: endogenous and exogenous components. J Zool 196:489–497

    Article  CAS  Google Scholar 

  • Goldstien SJ, Schiel DR, Gemmell NJ (2010) Regional connectivity and coastal expansion: differentiating pre-border and post-border vectors for the invasive tunicate Styela clava. Mol Ecol 19:874–885

    Article  CAS  Google Scholar 

  • Gust N, Inglis GJ, Floerl O, Peacock L, Denny C, Forrest B (2009) Assessment of population management options for Styela clava. In: MAFBNZ (ed) MAFBNZ Technical Paper. MAFBNZ, Wellington, p 237

  • Holmes NJ (1969) Aspects of the biology of Styela clava Herdman. PhD Thesis. University of Southampton, Southampton

  • Humason GL (1972) Animal tissue techniques, 3rd edn. W.H. Freeman, San Francisco

    Google Scholar 

  • Jiang A-L, Yu Z, Cai W-G, Wang C-H (2008) Feeding selectivity of the marine ascidian Styela clava. Aquac Res 39:1190–1197

    Article  Google Scholar 

  • Kelly DL (1974) Aspects of the reproductive ecology of three solitary ascidians: Ciona intestinalis (L.), Styela plicata (Les.), and Styela clava (H.) from southern California. MA thesis, California State University, Fullerton

  • Kluza D, Ridgway I, Kleeman S, Gould B (2006) Organism impact assessment: Styela clava (Clubbed Tunicate). Biosecurity New Zealand, Version 20/10/2006

  • Korringa P (1947) Relations between the moon and periodicity in the breeding of marine animals. Ecol Monogr 17:347–381

    Google Scholar 

  • Kott P (1985) The Australian Ascidiacea. Part I, Phlebobranchia and Stolidobranchia. Mem Queensl Mus 23:1–440

    Google Scholar 

  • Lambert C (2005a) Signaling pathways in ascidian oocyte maturation: effects of various inhibitors and activators on germinal vesicle breakdown. Develop Growth Differ 47:265–272

    Article  CAS  Google Scholar 

  • Lambert G (2005b) Ecology and natural history of the protochordates. Can J Zool 83:34–50

    Article  Google Scholar 

  • Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4

    Article  Google Scholar 

  • Lambert CC, Brandt CL (1967) The effect of light on the spawning of Ciona intestinalis. Biol Bull 132:222–228

    Article  Google Scholar 

  • Lambert CC, Lambert G (1998) Non‐indigenous ascidians in southern California harbors and marinas. Mar Biol 130:675–688

    Google Scholar 

  • Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161

    Article  Google Scholar 

  • Lambert G, Lambert CC, Abbott DP (1981) Corella species in the American Pacific Northwest: distinction of C. inflata Huntsman, 1912 from C. willmeriana Herdman, 1898 (Ascidiacea, Phlebobranchia). Can J Zool 59:1493–1504

    Google Scholar 

  • Lützen J (1999) Styela clava Herdman (Urochordata, Ascidiacea), a successful immigrant to North‐West Europe: ecology, propagation and chronology of spread. Helgolander Meeresun 52:383–391

    Article  Google Scholar 

  • Lützen J, Sørensen V (1993) Udbredelse, okologi og forplantning i Danmark af den indsleebte sopung, Styela clava Herdman. Flora Fauna 99:75–79 (in Danish, with an English summary)

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasion: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Manríquez PH, Castilla JC (2005) Self‐fertilization as an alternative mode of reproduction in the solitary tunicate Pyura chilensis. Mar Ecol Prog Ser 305:113–125

    Article  Google Scholar 

  • McClary D, Phipps C, Hinni S (2008) Reproductive behavior of the Clubbed Tunicate, Styela clava, in northern New Zealand waters. BRP 186/2005. MAF Biosecurity New Zealand. Technical Paper No: 2009/01. ISBN 978-0-478-33838-6

  • Minchin D, Duggan CB (1988) The distribution of the exotic ascidian, Styela clava Herdman, in Cork Harbour. Ir Nat J 22:388–393

  • Morris RH, Abbott DA, Haderlie EC (1980) Intertidal Invertebrates of California. Stanford University Press, Stanford

    Google Scholar 

  • Nandakumar K, Tanaka M, Kikuchi T (1993) Interspecific competition among fouling organisms in Tomioka Bay, Japan. Mar Ecol Prog Ser 94:43–50

    Article  Google Scholar 

  • Naylor E (2001) Marine animal behaviour relation to lunar phase. Earth Moon Planets 85–86:291–302

    Google Scholar 

  • Olive PJW (1995) Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J Therm Biol 20:79–90

    Google Scholar 

  • Orton JH (1920) Sea temperature, breeding and distribution in marine animals. J Mar Biol Assoc UK 12:339–336

    Google Scholar 

  • Osman RW, Whitlatch RB (1999) Ecological interactions of invading ascidians within epifaunal communities of southern New England. Marine Bioinvasions. In: Proceedings of a conference January 24–27, 1999, MIT, Cambridge, MIT Sea Grant College Program, pp 164–174

  • Osman RW, Whitlatch RB, Zajac RN (1989) Effects of resident species on recruitment into a community: larval settlement versus post‐settlement mortality in the oyster Crassostrea virginica. Mar Ecol Prog Ser 54:61–73

    Google Scholar 

  • Panagiotou M, Antoniadou C, Chintiroglou C (2008) Population dynamics and reproductive status of Microcosmus savignyi Monniot, 1962 (Thermaikos Gulf, Eastern Mediterranean): a preliminary assessment. J Nat Hist 42:545–558

    Google Scholar 

  • Parker LE, Culloty S, O’Riordan RM, Kelleher R, Steele S, Van der Velde G (1999) Preliminary study on the gonad development of the exotic ascidian Styela clava in Cork Harbour. J Mar Biol Assoc UK 79:1141–1142

    Google Scholar 

  • Ricciardi A, Rasmussen JB (1998) Predicting the identity and impact of future biological invaders: A priority for aquatic resource management. Can J Fish Aquat Sci 55:1759–1765

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Co, New York

    Google Scholar 

  • Stuart V, Klumpp DW (1984) Evidence for food resource partitioning by the kelp-bed filter feeders. Mar Ecol Prog Ser 16:27–37

    Article  Google Scholar 

  • Thompson RC, MacNair N (2004) An overview of the clubbed tunicate (Styela clava) in Prince Edward Island. PEI Department of Agriculture, Fisheries, Aquaculture and Forestry Technical Report, vol 234, p 29

  • Wallace H (1961) The breeding and development of Styela mammiculata Carlisle. J Mar Biol Assoc UK 41:187–190

    Article  Google Scholar 

  • Wasson K, Zabin CJ, Bedinger L, Diaz MC, Pearse JS (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biol Conserv 102:143–153

    Google Scholar 

  • Watanabe H, Lambert CC (1973) Larva release in response to light by the compound ascidians Distaplia occidentalis and Metandrocarpa taylori. Biol Bull 144:556–566

    Article  Google Scholar 

  • West AB, Lambert CC (1976) Control of spawning in the tunicate Styela plicata by variation in a natural light regime. J Exp Zool 195:263–270

    Article  Google Scholar 

  • Whittingham DG (1967) Light induction of shedding of gametes in Ciona intestinalis and Molgula manhattensis. Biol Bull 132:292–296

    Article  CAS  Google Scholar 

  • Yoshida M (1952) Some observations on the maturation of the sea urchin, Diadema setosum. Annot Zool Japan 25:265–271

    Google Scholar 

  • Zajac RN, Whitlatch RB, Osman RW (1989) Effects of inter‐specific density and food supply on survivorship and growth of newly settled benthos. Mar Ecol Prog Ser 56:127–132

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Upper Saddle River, New York

    Google Scholar 

  • Zeldis JR, Oldman J, Ballara SL, Richards LA (2005) Physical fluxes, pelagic ecosystem structure, and larval fish survival in Hauraki Gulf, New Zealand. Can J Fish Aquat Sci 62:593–610

    Article  Google Scholar 

Download references

Acknowledgments

Funding for research was provided by Biosecurity New Zealand (to D. McClary) and the University of Auckland. Thanks to Adrian Turner for assistance with microscopy, Todd Denis and Louis Ranjard for statistical advice and the management of Bayswater Marina to permit the collection of samples. We also thank our three anonymous reviewers whose suggestions improved the manuscript.

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand

    Nicholas A. Wong & Mary A. Sewell

  2. Golder Associates (NZ) Limited, Level 2, Takapuna Business Park, 4 Fred Thomas Drive, Takapuna, Auckland, 0740, New Zealand

    Dan McClary

  3. Sinclair Knight Merz, Level 7, Durack Centre, 263 Adelaide Terrace, Perth, WA, 6001, Australia

    Dan McClary

Authors
  1. Nicholas A. Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dan McClary
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mary A. Sewell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicholas A. Wong.

Additional information

Communicated by S. Connell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wong, N.A., McClary, D. & Sewell, M.A. The reproductive ecology of the invasive ascidian, Styela clava, in Auckland Harbour, New Zealand. Mar Biol 158, 2775–2785 (2011). https://doi.org/10.1007/s00227-011-1776-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1776-6

Keywords

Search

Navigation